Comparative genomics of biotechnologically important yeasts

Abstract

Ascomycete yeasts are metabolically diverse, with great potential for biotechnology. Here, we report the comparative genome analysis of 29 taxonomically and biotechnologically important yeasts, including 16 newly sequenced. We identify a genetic code change, CUG-Ala, in Pachysolen tannophilus in the clade sister to the known CUG-Ser clade. Our well-resolved yeast phylogeny shows that some traits, such as methylotrophy, are restricted to single clades, whereas others, such as L-rhamnose utilization, have patchy phylogenetic distributions. Gene clusters, with variable organization and distribution, encode many pathways of interest. Genomics can predict some biochemical traits precisely, but the genomic basis of others, such as xylose utilization, remains unresolved. Our data also provide insight into early evolution of ascomycetes. We document the loss of H3K9me2/3 heterochromatin, the origin of ascomycete mating-type switching, and panascomycete synteny at the MAT locus. These data and analyses will facilitate the engineering of efficient biosynthetic and degradative pathways and gateways for genomic manipulation.genomics | bioenergy | biotechnological yeasts | genetic code | microbiology Y easts are fungi that reproduce asexually by budding or fission and sexually without multicellular fruiting bodies (1, 2). Their unicellular, largely free-living lifestyle has evolved several times (3). Despite morphological similarities, yeasts constitute over 1,500 known species that inhabit many specialized environmental niches and associations, including virtually all varieties of fruits and flowers, plant surfaces and exudates, insects and other invertebrates, birds, mammals, and highly diverse soils (4). Biochemical and genomic studies of the model yeast Saccharomyces cerevisiaeessential for making bread, beer, and wine-have established much of our understanding of eukaryotic biology. However, in many ways, S. cerevisiae is an oddity among the yeasts, and many important biotechnological applications and highly divergent physiological capabilities of lesser-known yeast species have not been fully exploited (5). Various species can grow on methanol or n-alkanes as sole carbon and energy sources, overproduce vitamins and lipids, thrive under acidic conditions, and ferment unconventional carbon sources. Many features of yeasts make them ideal platforms for biotechnological processes. Their thick cell walls help them survive osmotic shock, and in contrast to bacteria, they are resistant to viruses. Their unicellular form is easy to cultivate, scale up, and harvest. The objective of this study was, therefore, to put yeasts with diverse biotechnological applications in a phylogenomic context and relate their physiologies to genomic SignificanceThe highly diverse Ascomycete yeasts have enormous biotechnological potential. Collectively, these yeasts convert a broad range of substrates into useful compounds, such as ethanol, lipids, and vitamins, and can grow in extremes of temperature, salinity, and pH. We compared 29 yeast genome...

Genetic basis of priority effects: insights from nectar yeast

“…However, a third Ser-identity element, G3C3 run in the variable loop, is missing similar to M. bicuspidata. This supports the recently proposed stepwise accumulation of tRNA CAG Ser features in the evolution of alternative CUG translation [23]. Alignment of conserved CUG-sites further supports the alternative codon usage in M. reukaufii.…”

“…EST evidence from M. fructicola and M. bicuspidata was used to train MAKER [23,45]. Protein evidence from M. bicuspidata, D. hansenii, Candida tenuis and C. lusitaniae were also used [23,44,46] We selected a range of species in a closely related sister clade (CUG-Ser) for which published genomes were available, other ascomycetous nectar yeasts, and the manually created reference genome of S. cerevisiae in order to evaluate the assembly completeness of M. reukaufii genome, using CEGMA genes as reference. Blast2GO (v. 2.7.2) [47] was used with BLASTP searches against the NCBI fungi dataset, filtered using Blast2GO annotation algorithm, and GO, and enzyme code were annotated using the GO database.…”

Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network

“…The genes encoding the Leloir enzymes occur in one of the few broadly conserved yeast gene clusters (Wong and Wolfe, 2005; Slot and Rokas, 2010; Wolfe et al, 2015; Riley et al, 2016), which has been suggested could promote enzyme co-regulation to prevent the accumulation of toxic intermediates (Price et al, 2005; Lang and Botstein, 2011) or ensure that only complete networks are co-inherited (Lawrence and Roth, 1996; Hittinger et al, 2010). In addition to S. uvarum , many yeast species that underwent the WGD retain GAL80B (Hittinger et al, 2004).…”

“…In addition to S. uvarum , many yeast species that underwent the WGD retain GAL80B (Hittinger et al, 2004). Perhaps due to these intrinsic metabolic challenges and the limited benefits of maintaining a dedicated GAL network, the ability to consume galactose has been lost many times across diverse yeast lineages (Hittinger et al, 2004, 2015; Slot and Rokas, 2010; Wolfe et al, 2015; Riley et al, 2016). …”

How tRNAs dictate nuclear codon reassignments: Only a few can capture non-cognate codons

“…However, studies of mitochondrial genomes in the last 10 y and recent discoveries of codon reassignments in nuclear genomes showed that all reassignments including the yeast CUG codon alteration are highly polyphyletic and include multiple amino acids. [17][18][19][20][21][22][23] Reassignments in species such as Blastocrithidia species 24 and Amoeboaphelidium protococcarum 25 currently appear to be isolated events. Sequencing of further, related species might lead to reconsolidation.…”